Environmental Biology of Fishes

, Volume 96, Issue 6, pp 701–712 | Cite as

Hidden mitochondrial DNA divergence in the Lake Biwa endemic goby Gymnogobius isaza: implications for its evolutionary history

Article

Abstract

The gobiid Gymnogobius isaza is an endemic species that has adapted remarkably to the pelagic environment in Lake Biwa, Japan, a representative ancient lake in East Asia. To obtain clues that would reveal the origin and evolution of this species, we conducted phylogenetic and population genetic analyses based on partial sequences of the mitochondrial cytochrome b gene. Consistent with previous studies, our Bayesian phylogenetic analysis with a relaxed molecular clock model reconfirmed a sister relationship between G. isaza and Gymnogobius urotaenia + Gymnogobius petschiliensis, with a divergence time of about 2.9 million years (Myr), and provided an evolutionary rate of 3.0 %/Myr (pairwise) for their clade. Population genetic analysis revealed two distinct mtDNA groups in G. isaza, which were estimated to have diverged 0.66 million years ago (Mya) at the Lake Katata stage of Paleo-Lake Biwa, preceding the origin of the present Lake Biwa environment with its extensive deep pelagic area (0.3–0.4 Mya). A dumbbell-like haplotype network and bimodal mismatch distribution suggested that the population of G. isaza experienced secondary contact between two genetically differentiated populations. Demographic parameters from mismatch distribution analysis and Bayesian skyline plot analysis suggested that both of the mtDNA groups of G. isaza exhibited a signal of sudden population expansion at approximately the same time (80–90 thousand years ago) during the last glacial period after the development of the present Lake Biwa. These results imply the complex population history of G. isaza, including genetic isolation and secondary contact following differentiation from its relatives in the Pliocene.

Keywords

Gymnogobius Mitochondrial DNA Lake Biwa Historical demography Divergence time 

Notes

Acknowledgments

We are grateful to T. Komiya, R. Kakioka, K. Tominaga, and the members of the Laboratory of Animal Ecology at Kyoto University for providing specimens and helpful comments, and to professional fishermen of Lake Biwa for their cooperation in fish sampling. This study was supported in part by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology, Japan (nos. 18570086, 21370035, and “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem” of the GCOE) and the WEC Research Fund for Ecology and Civil Engineering (2009-6).

References

  1. Aizawa T, Hatsumi M, Wakahama K (1994) Systematic study on the Chaenogobius species (family Gobiidae) by analysis of allozyme polymorphisms. Zool Sci 11:455–465Google Scholar
  2. Aoyama J, Watanabe S, Ishikawa S, Nishida M, Tsukamoto K (2000) Are morphological characters distinctive enough to discriminate between two species of freshwater eels, Anguilla celebesensis and A. interioris? Ichthyol Res 47:157–161CrossRefGoogle Scholar
  3. Avise JC (2000) Phylogeography: the history and information of species. Harvard Univ. Press, CambridgeGoogle Scholar
  4. Briolay J, Galtier N, Brito RM, Bouvet Y (1998) Molecular phylogeny of Cyprinidae inferred from cytochrome b DNA sequences. Mol Phylogenet Evol 9:100–108PubMedCrossRefGoogle Scholar
  5. Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Mol Biol Evol 25:624–633PubMedCrossRefGoogle Scholar
  6. Clark PU, Alley RB, Pollard D (1999) Northern hemisphere ice-sheet influences on global climate change. Science 286:1104–1111CrossRefGoogle Scholar
  7. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660PubMedCrossRefGoogle Scholar
  8. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214PubMedCrossRefGoogle Scholar
  9. Drummond AJ, Suchard MA (2010) Bayesian random local clocks, or one rate to rule them all. BMC Biol 8:114PubMedCrossRefGoogle Scholar
  10. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192PubMedCrossRefGoogle Scholar
  11. Edwards SV, Beerli P (2000) Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54:1839–1854PubMedGoogle Scholar
  12. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567PubMedCrossRefGoogle Scholar
  13. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  14. Garber AF, Tringali MD, Franks JS (2005) Population genetic and phylogeographic structure of wahoo, Acanthocybium solandri, from the western central Atlantic and central Pacific Oceans. Mar Biol 147:205–214CrossRefGoogle Scholar
  15. Harada S, Jeon SR, Kinoshita I, Tanaka M, Nishida M (2002) Phylogenetic relationships of four species of floating gobies (Gymnogobius) as inferred from partial mitochondrial cytochrome b gene sequences. Ichthyol Res 49:324–332CrossRefGoogle Scholar
  16. Harpending H (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedGoogle Scholar
  17. Hidaka T, Takahashi S (1987) Reproductive strategy and interspecific competition in the lake-living gobiid fish Isaza, Chaenogobius isaza. J Ethol 5:185–196CrossRefGoogle Scholar
  18. Hirase S, Ikeda M, Kanno M, Kijima A (2012) Phylogeography of the Phylogeography of the intertidal goby Chaenogobius annularis associated with paleoenvironmental changes around the Japanese Archipelago. Mar Ecol Prog Ser 450:167–179CrossRefGoogle Scholar
  19. Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568PubMedCrossRefGoogle Scholar
  20. Hosoya K (1987) Phylogeny and character displacement in Gnathopogon fishes. In: Mizuno N, Goto A (eds) Freshwater fishes in Japan: their distribution, variation and speciation. Tokai University Press, Tokyo, pp 31–40 (in Japanese)Google Scholar
  21. Kawabe T (1994) Chapter 1. Biwako no Oitachi (formation of Lake Biwa). In: Research Group for Natural History of Lake Biwa (ed) Biwako no Shizenshi (The natural history of Lake Biwa). Yasaka Shobo, Tokyo, pp 24–72 (in Japanese)Google Scholar
  22. Kawanabe H (1978) Some biological problems. Verh Internat Ver Limnol 20:2674–2677Google Scholar
  23. Kawanabe H (1996) Asian great lakes, especially Lake Biwa. Environ Biol Fish 47:219–234CrossRefGoogle Scholar
  24. Kitamura A, Takano O, Takata H (2001) Late Pliocene early Pleistocene paleoceanographic evolution of the Sea of Japan. Palaeogeogr Palaeoclimatol Palaeoecol 172:81–98CrossRefGoogle Scholar
  25. Komiya T, Fujita S, Watanabe K (2011) A novel resource polymorphism in fish, driven by differential bottom environments: an example from an ancient lake in Japan. PLoS One 6:e17430PubMedCrossRefGoogle Scholar
  26. Magoulas A, Tsimenides N, Zouros E (1996) Mitochondrial DNA phylogeny and the reconstruction of the population history of a species: the case of the European anchovy (Engraulis encrasicolus). Mol Biol Evol 13:178–190PubMedCrossRefGoogle Scholar
  27. Meyers PA, Takemura K, Horie S (1993) Reinterpretation of late Quaternary sediment chronology of Lake Biwa, Japan, from correlation with marine glacial–interglacial cycles. Quat Res 39:154–162CrossRefGoogle Scholar
  28. Miya M, Nishida M (2000) Use of mitogenomic information in teleostean molecular phylogenetics: a tree-based exploration under the maximum-parsimony optimality criterion. Mol Phylogenet Evol 17:437–455PubMedCrossRefGoogle Scholar
  29. Nakajima T (1994) Chapter 2–4 (d). Cyprinid fishes. In: Research Group for Natural History of Lake Biwa (ed) Biwako no Shizenshi (The natural history of Lake Biwa). Yasaka Shobo, Tokyo, pp 235–275 (in Japanese)Google Scholar
  30. Nishino M (2003) Biwako no Koyushu wo Meguru Mondai. Koyushu list no Ichibu Shusei nit suite (The problem of endemics in Lake Biwa). Oumia 76:3–4 (in Japanese)Google Scholar
  31. Nishino M, Hamabata E (2005) Naiko karano Message (The message from “Naiko (lagoon around Lake Biwa)”). Sunrise Press, Shiga (in Japanese)Google Scholar
  32. Rambaut A (2009) FigTree Version 1.3.1. http://tree.bio.ed.ac.uk/software/figtree/
  33. Rambaut A, Drummond AJ (2009) Tracer Version 1.5. http://tree.bio.ed.ac.uk/software/tracer/
  34. Rogers AR, Harpending H (1992) Population growth makes waxes in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  35. Rossiter A (2000) Lake Biwa as a topical ancient Lake. Adv Ecol Res 31:571–598CrossRefGoogle Scholar
  36. Seehausen O (2006) African cichlid fish: a model system in adaptive radiation research. Proc R Soc B 273:1987–1998PubMedCrossRefGoogle Scholar
  37. Slatkin M, Hudson R (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562PubMedGoogle Scholar
  38. Slobodyanyuk SJ, Kirichik SV, Pavlova ME, Belikov SI, Novitsky AL (1995) The evolutionary relationships of two families of Cottoid Fishes of Lake Baikal (East Siberia) as suggested by analysis of mitochondrial DNA. Mol Evol 40:392–399CrossRefGoogle Scholar
  39. Sota T, Mukai T, Shinozaki T, Sato H, Yodoe K (2005) Genetic differentiation of the gobies Gymnogobius castaneus and taranetzi in the region surrounding the Sea of Japan as inferred from a mitochondrial gene genealogy. Zool Sci 22:87–93PubMedCrossRefGoogle Scholar
  40. Tada R (1994) Paleoceanographic evolution of the Japan Sea. Palaeogeogr Palaeoclimatol Palaeoecol 108:487–508CrossRefGoogle Scholar
  41. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  42. Takahashi S (1981) Vertical distribution and diel migration of Isaza, Chaenogobius isaza, Pisces in Lake Biwa. Zool Mag 90:265–270Google Scholar
  43. Takahashi S (1989) A review of the origins of endemic species in Lake Biwa with special reference to the goby fish, Chaenogobius isaza. J Paleolimnology 1:279–292CrossRefGoogle Scholar
  44. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  45. Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional, and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Resour 11:914–921PubMedCrossRefGoogle Scholar
  46. Tokui T, Kawanabe H (1984) Fishes. In: Horie S (ed) Lake Biwa, Monographiae Biologicae, vol 54. Dr W Junk Publishers, Dordrecht, pp 339–360Google Scholar
  47. Tomoda Y (1978) Biwako to namazu (Lake Biwa and catfish). Chobunsha, Tokyo (in Japanese)Google Scholar
  48. Walstrom WV, Klicka J, Spellman GM (2012) Speciation in the white-breasted nuthatch (Sitta carolonensis): a multilocus perspective. Mol Ecol 21:907–920PubMedCrossRefGoogle Scholar
  49. Watanabe K, Mori S (2008) Comparison of genetic population structure between two cyprinids, Hemigrammocypris rasborella and Pseudorasbora pumila subsp., in the Ise Bay basin, central Honshu, Japan. Ichthyol Res 55:309–320CrossRefGoogle Scholar
  50. Watanabe K, Takahashi H (2010) Tansuigyorui chiri no shizenshi (Natural history of freshwater fish geography). Hokkaido University Press, Sapporo (in Japanese)Google Scholar
  51. Watanabe K, Kano Y, Takahashi H, Mukai T, Kakioka R, Tominaga K (2010a) GEDIMAP: a database of genetic diversity for Japanese freshwater fishes. Ichthyol Res 57:107–109CrossRefGoogle Scholar
  52. Watanabe K, Kawase S, Mukai T, Kakioka R, Miyazaki J-I, Hosoya K (2010b) Population divergence of Biwia zezera (Cyprinidae: Gobioninae) and the discovery of a cryptic species, based on mitochondrial and nuclear DNA sequence analyses. Zool Sci 27:647–655PubMedCrossRefGoogle Scholar
  53. Yokoyama T (1984) Stratigraphy of the Quaternary system around Lake Biwa and geohistory of the ancient Lake Biwa. In: Horie S (ed) Lake Biwa, Monographiae Biologicae, vol 54. Dr W Junk Publishers, Dordrecht, pp 43–128Google Scholar
  54. Yokoyama Y, Lambeck K, De Deckker P, Johnston P, Fifield LK (2000) Timing of the Last Glacial Maximum from observed sea-level minima. Nature 406:713–716PubMedCrossRefGoogle Scholar
  55. Yonekura N, Kaizuka S, Nogami M, Chinzai K (2001) Regional geomorphology of the Japanese Islands, vol 1 Introduction to Japanese geomorphology. University of Tokyo Press, Tokyo (in Japanese)Google Scholar
  56. Yuma H, Hosoya K, Nagata Y (1998) Distribution of the freshwater fishes of Japan: an historical overview. Environ Biol Fish 52:97–124CrossRefGoogle Scholar
  57. Zardoya R, Doadrio I (1999) Molecular evidence on the evolutionary and biogeographical pattern of European cyprinids. J Mol Evol 49:227–237PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Graduate School of ScienceKyoto UniversityKyotoJapan

Personalised recommendations